Adaptive Bleaching Hypothesis (2)

[Ove Hoegh-Guldberg]

Dear Coral-list,

I hope that it is not inappropriate to provoke discussion about this much
talked about topic.  My sole intention is to explore this important issue.  
I have chosen to deal with it as a series of carefully defined steps.  As
will you see, while the theory may have logical appeal, the critical
assumptions upon which it is based are either false or unsubstantiated.

Before I begin, a clarification with respect to the biological terms
"adaptation' and "acclimation".  Adaptation is strictly used to describe
genetic changes in a population that lead to genetically based
characteristics of that population considered more optimal with respect to
the local environment. Acclimation refers to phenotypic change whereby
(through changes in gene expression and/or post-translational
modification) the characteristics of an organism are made more optimal
relative to the local environment.  These definitions are held by most
textbooks (e.g. Eckert and Randall etc) and are not mutable (as far as I
know).

The Adaptive Bleaching Hypothesis (ABH)

In order to proceed logically, exploring the assumptions of the hypothesis
makes good sense.  These are listed by Ware, Fautin and Buddemeier (1996;
Patterns of coral bleaching: modelling the adaptive bleaching hypothesis",
Ecol. Modelling 84:199-214).  I find this paper useful because it lists
the five critical assumptions of the ABH and then builds a logical model
from this grounding, the behaviour of which can be compared to nature.  
As with any model, however, the assumptions (assuming correct logical
deductive processes) are critical for the truth of a model (to state the
obvious, if the assumptions are wrong, then the model or argument fails).

Summary table (details below):

  a.. Assumption 1 =  true
  b.. Assumption 2 =  false at the time scale required
  c.. Assumption 3 =  true
  d.. Assumption 4 =  false
  e.. Assumption 5 =  false if assumption 4 is false

Conclusion (details below):

Critical assumptions 2 and 4 (5 depends on 4) are not currently supported
and available evidence (little evidence to the contrary) suggests that
they are false.  From this analysis, the only conclusion is that the ABH
is false.

Details:

What are the assumptions of Ware, Fautin and Buddemeier (1996) and are
they true or false?

Assumption 1.  "Multiple types of both zooxanthellae and host species
commonly exist on a coral reef."

This is true for corals and work by Trench, Rowan, Loh, Baker, Loi, Carter
and others have shown that it is true for zooxanthellae (i.e. diversity is
high among zooxanthellae).

Assumption 2.  'Some types of zooxanthellae are able to live with more
than one host species, and host species may form symbiotic relationships
with more than one type of zooxanthella, either simultaneously or
serially.  The various combinations differ in their adaptation to the
environment."

As you will see from the following, this is false at the timescale
required. Other critical pieces of evidence do not exist.

What is true: Some types of zooxanthellae (distinguished via rDNA
sequences - note - RFLPs do not have enough precision to distinguish
species etc) appear in several corals while other coral species have their
own dedicated zooxanthella type (Rowan, Wilcox, Baker, Loh and others, Loh
et al. in press).  Some hosts show several different rDNA sequences
associated with their zooxanthellae (Rowan and Powers 1991, Rowan 1998).  
There is evidence that some zooxanthellae may specialise in high light or
low light habitats (e.g. Rowan et al 1997, see also recent papers by K.
Michalek-Wagner, A Banazak re: different zooxanthella biochemistries) -
and it is likely that various combinations of host and symbiont differ in
the type or quality of the environment that they are adapted for.  
Specific evidence about heat tolerance of different combinations is
lacking although Kinzie et al 2001, Iglesias-Prieto and others have some
evidence that different isolated zooxanthellae have different heat
tolerances (but see Assumption 3 which states that the tolerance of the
host-symbiont combination is all important).

What is unknown: How mutable (changed) are these relationships?  An
important part of this assumption for the ABH is that new symbiotic
relationships can form and disband over very short periods of time.  
Without this rapid, dynamic feature bleaching will not be important
mechanism for the evolution of new combinations.  If they are not easily
mutable then the long-term performance of different strain and host
combinations under new conditions and their impact on reproductive success
of both partners etc. through reduced energy and other inputs will be more
important.

Evidence that this is assumption is largely untrue at the time scales
needed: To my knowledge, no lab or field infection experiment using
dinoflagellates from other hosts (like those of WK Fitt and others) have
ever resulted in a new combination of symbiotic algae and host.  In cases
where foreign types of zooxanthellae were introduced, populations were
eventually replaced by the original type of zooxanthella (see also Kinzie
and partners 2001, who also obtained this result with field exposed,
completely aposymbiotic anemones). Also - no one has seen a change in the
types of zooxanthellae occupied by a coral following a bleaching event
(i.e. new combinations arising from a bleaching event).  Baker (2001)'s
techniques do not have the necessary resolution to answer this question.  
He sees new bands arise within the zooxanthellae isolated within corals
translocated to the shallows.  However, he cannot say that the new bands
are due to invasion of external zooxanthellae or a case of up-regulation
of a small existing population of the particular type of zooxanthellae
concerned (he would have to clone his PCR products and verify for a large
number of transformed clones that there were no sequences - hence
zooxanthellae cells - of the new RFLP band in his corals before treatment
i.e. that the change is not a product of acclimation as opposed to
adaptation).

Implications:  The process of symbiont switching operates at a longer time
scale making bleaching irrelevant to the process.  This is not surprising
if the complex requirements of integrating two genomes into a symbiosis
are considered. Research on what is required reveals complex self-non-self
recognition (McNeil, P. L., T. Colley, Trench, Hohman, et al. (1981). J.
Cell Sci. 52: 243-270, Muscatine, Hohman and others), metabolite transfer
and the host of other specific lock-and-key biochemical and physiological
interactions.  We need to think of transferring zooxanthellae between
hosts as partly akin to transplanting chloroplasts or mitochondria between
plant species.  Remember also that the types of zooxanthellae that occupy
different corals are quite separate genetically and may represent
different species or even genera (Trench, McNally et al. 1994 and others)
- hence are likely to have a large suite of different requirements and
features that have to be integrated (evolved) in order for a symbiosis to
function.  Adopting life within another cellular environment is not
trivial and may involve many coordinated changes in genetic makeup (aka it
is not simple to swap from one host to another - hence this process is
likely to constrained in terms of evolutionary speed).

If new zooxanthellae types cannot invade easily, then the ABH is
restricted to the dynamics of the zooxanthella populations of a subset of
corals which already have multiple strains of zooxanthellae in their
tissues.  That is, new combinations do not form "easily" (at the very
least, they probably form over decades to centuries but not over the days
and weeks required by the ABH).  At this point, we are left with changes
that occur in the relative frequency of existing genotypes within a coral.  
These are pre-existing genetic combinations. The question at this point
becomes, is this "adaptation" or "acclimation"?  At first cut - one might
call this is "adaptation" because there is a change in the frequency of
genotypes within the total zooxanthella population of an geographic area.

This is wrong, however, as populations of zooxanthellae within a host are
largely clonal (asexual) populations of single individuals.  If this is
the case, then a multi-strain coral host is really an association of three
or more individuals (the coral host individual, and 2 or more zooxanthella
individuals). The change in the relative proportions of one zooxanthellae
individual over another within a host is then a matter of a change in the
size of individuals. This then is a phenotypic (acclimatory) not genotypic
(adaptive) change.  Being multistrained and responding to changed
circumstances, then, is no different to a association that having a set
range of phenotypic responses with definite limits (there is no such thing
as unlimited acclimation).  Perhaps in evolutionary time (at least decades
to centuries), the switching of symbionts may allow a certain flexibility
that is not inherent within a single genome. But the time scale and
process do not involve bleaching (adaptive or acclimatory).

Assumption 3.  "The upper temperature limit beyond which the symbiosis is
disrupted is characteristic of the host-symbiont combination rather than
of the host or symbiotic alga alone."

This is probably true given the highly integrated nature of symbiosis.  
Specific thermal tolerances of corals/zooxanthellae associations and their
variance with thermal regimes were largely first identified by Steve Coles
and Paul Jokiel. Many recent studies (Goreau, Strong, Hayes, Brown)
culminating in the SST and HotSpot work by NOAA and others.  New work by
Ray Berkelmans (in press) further confirms that thermal tolerances vary on
a geographic basis with water temperature.

Assumption 4. "Bleaching provides an opportunity for the host to be
repopulated with a different type of partner."

This is unproven and most evidence suggests that it is false.  As I have
repeatedly stated, we have yet to see a single experiment that shows that
a bleaching event or set of disturbances results in a change of the type
of symbiont with corals (during or after).  No one has evidence of a more
fit recombination of host and symbiont as a result of changed
circumstances.  Even the recent Kinzie el al (2001) study with
aposymbionts of the sea anemone (Aiptasia) found that they did not take up
new types of zooxanthellae.  Apart from the problem of having very limited
genetic resolution due to limitations of the RFLP technique (same problem
as with AC Baker's 2001 study), Kinzie and co.'s aposymbiotic anemone
hosts only became infected by the original type (B) of zooxanthella (To
quote them: "All Aiptasia that became infected when exposed to natural
seawater were found to harbour clade B, which is the zooxanthellar clade
normally found in this anemone").

Unfortunately for the ABH, other observations militate against this
assumption being true:

Firstly, corals that appear totally white still have many zooxanthellae in
their tissues (e.g. Hoegh-Guldberg and Salvat 1995 - bone white corals
ranged as high as 1.0 x 104 cell/cm2). These are probably the source of
repopulation of corals by zooxanthellae in the event of recovery after
bleaching.  If competition by the original zooxanthellae is so effective
(i.e. "originals" win every time according to WK Fitt, D Schoenberg and
others who have done the rigorous experiments in this regard), then it
would appear that this is a major obstacle to the idea that "bleaching
provides an opportunity for the host to be repopulated with a different
type of partner."  That is, bleaching does not make a coral or other
cnidarian host an open slate.  The inherent algae in recovering corals
probably will always have the upper hand.

Secondly, as stated above, no one has seen a single case of bleaching
providing "an opportunity for the host to be repopulated with a different
type of partner".  If this were a major forcing function within the
evolution of coral reefs, shouldn't we see large scale examples of this?  
William Loh from my lab has been searching for changes in rDNA sequence
types of zooxanthellae with corals and reefs after bleaching events in
Okinawa with his Japanese colleagues. What he has seen is potential
selection against some zooxanthella genotypes and associations (their
coral host species died out) but never the advent of a new association of
host and symbiont.  That is, on the short term scales of bleaching events,
William has seen a diminishing not increasing stock of combinations (not
good for adaptation as you will appreciate).  At risk of repeating myself,
the advent of new combinations probably requires a longer time period
(because of the biochemical complexities of symbiosis) than the few
generation times required. See above.

An added assumption is added by the authors under assumption 4.  They
state: "We assume no mortality of bleached corals, regardless of the
severity of bleaching or whether there is a zooxanthella type with which
the coral is compatible under the existing temperature conditions."

I assume that this addition is a condition for the computer model to work.  
In the face of overwhelming field evidence, this is simply false (GCRMN,
Wilkinson and many others).  A model that requires this falls over heavily
at this point. Perhaps John can explain how critical this element is and
how dependent the ABH is on it.

Assumption 5.  "Stress-sensitive combinations have competitive advantages
in the absence of stress, which implies a reversion to stress-prone
combinations under non-stressful conditions."

This remains unknown.  However, if we haven't seen assumption 4 holding
true (i.e. that bleaching leads to new fitter combinations), then we
obviously don't have assumption 5 (the reversion of these combinations in
periods of non-stress) in the bag.

In conclusion:

The ABH has more than a few problems in terms of the stated assumptions
and should be discarded.  It was a "nice" idea but now is largely
falsified through the fact that critical assumptions like 2 and 4 above
are (at the very least) false.

I hope that this helps progress the ABH debate in a positive way.  I am
very interested in engaging in discussions over the details above.  Most
of all - I want to strongly emphasize that this is not an attempt to
denigrate the ABH authors but more an attempt to improve our understanding
of mass bleaching by critically examining important ideas and suggestions.  
I am aware that coral-list members may have much to add and that I
probably have not done justice to all authors (if there are critical
pieces of literature, please bring them to the list's attention).

Regards to all,

Ove

Professor Ove Hoegh-Guldberg
Director, Centre for Marine Studies
University of Queensland
St Lucia, 4072, QLD

Phone:  +61 07 3365 4333
Fax:       +61 07 3365 4755
Email:    oveh at uq.edu.au
http://www.marine.uq.edu.au/staff/ohg.html

Great Barrier Reef Research Stations
http://www.marine.uq.edu.au/stations.html


~~~~~~~
For directions on subscribing and unsubscribing to coral-list or the
digests, please visit www.coral.noaa.gov, click on Popular on the
menu bar, then click on Coral-List Listserver.